Though avian skin is known to possess a highly lipogenic epidermis, little is known about its permeability barrier function. We correlated epidermal barrier function, fine structure and lipid biochemistry in the pigeon, Columbia livia, and compared these features with terrestrial mammalian systems. Whereas barrier function, as assessed by transepidermal water loss was not as efficient as in mammals, both groups shared certain morphological features including substantial compartmentalization of lipids in stratum corneum intercellular domains. Avian intercellular lipids derive from extrusion of intracellular non-membrane-bound droplets from lowermost corneocytes, rather than by secretion of lamellar discs from multigranular bodies, as previously reported in some avians, and in mammals. Instead, both the internal lamellae and the limiting membranes of multigranular bodies appear to degenerate, leading to the formation of non-membrane-bound droplets. The lipid content of avian epidermis and stratum corneum demonstrates important similarities to terrestrial mammals, i.e. abundant sphingolipids, a paucity of phospholipids, and abundant neutral lipids, but also certain striking differences, i.e. persistence of glycosphingolipids and triglycerides into the stratum corneum. Thus, avian stratum corneum forms a two-compartment system of lipid-depleted cells embedded in non-polar-lipid enriched intercellular domains, analogous to mammals. But, in contrast to mammals, the highly attenuated corneocytes of avians, which results from a paucity of keratin filaments, produce a 'straws-and-mortar' tissue, rather than the 'bricks-and-mortar' tissue of mammals.